Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense

Plant Physiology

Volumn 134, Issue 3, 2004, Pages 1027-1038

  Rouhier, Nicolas ^a   Gelhaye, Eric ^a   Gualberto, Jose M ^b   Jordy, Marie Noelle ^a   De Fay, Elisabeth ^a   Hirasawa, Masakazu ^c   Duplessis, Sebastien ^a   Lemaire, Stephane D ^d   Frey, Pascal ^e   Martin, Francis ^a   Manieri, Wanda ^f   Knaff, David B ^c   Jacquot, Jean Pierre ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b CNRS   (France)

^c TEXAS TECH UNIVERSITY   (United States)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^e CEMAGREF   (France)

^f Laboratoire de Biochimie   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CELLS; ENZYMES; FLUORESCENCE; HYDROGEN PEROXIDE;

GUARD CELLS; MUTANTS;

PLANTS (BOTANY);

BACTERIA (MICROORGANISMS); MELAMPSORA; MELAMPSORA LARICI-POPULINA; MELAMPSORA LARICIS-POPULINA; POPULUS; POPULUS BEROLINENSIS; POPULUS TREMULA; POPULUS TREMULOIDES; SPINACIA OLERACEA;

EID: 12144287638     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.103.035865     Document Type: Article

References (55)

1. Balmer Y, Schürmann P (2001) Heterodimer formation between thioredoxin f and fructose 1, 6-bisphosphatase from spinach chloroplasts. FEBS Lett 492: 58-61
2. Behm M, Jacquot JP (2000) Isolation and characterization of thioredoxin h from poplar xylem. Plant Physiol Biochem 38: 363-369
3. Brehelin C, Meyer EH, de Souris JP, Bonnard G, Meyer Y (2003) Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: similar sequences for divergent gene expression, protein localization, and activity. Plant Physiol 132: 2045-2057
4. Broin M, Cuine S, Eymery F, Rey P (2002) The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14: 1417-1432
5. Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407: 211-215
6. Capitani G, Markovic-Housley Z, DelVal G, Morris M, Jansonius JN, Schürmann P (2000) Crystal structures of two functionally different thioredoxins in spinach chloroplasts. J Mol Biol 302: 135-154
7. Chae HZ, Chung SJ, Rhee SG (1994a) Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem 269: 27670-27678
8. Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG (1994b) Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci USA 91: 7017-7021
9. Chivers PT, Prehoda KE, Raines RT (1997) The CXXC motif: a rheostat in the active site. Biochemistry 36: 4061-4066
10. Choi YO, Cheong NE, Lee KO, Jung BG, Hong CH, Jeong JH, Chi YH, Kim K, Cho MJ, Lee SY (1999) Cloning and expression of a new isotype of the peroxiredoxin gene of Chinese cabbage and its comparison to 2Cys-peroxiredoxin isolated from the same plant. Biochem Biophys Res Commun 258: 768-771
11. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98: 13454-13459
12. Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54: 93-107
13. Dietz KJ, Horling F, Konig J, Baier M (2002) The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. J Exp Bot 53: 1321-1329
14. 2 production, and peroxidase activity during the hypersensitive response to Xanthomonas campestris pv. vesicatoria in Capsicum annuum. Mol Plant-Microbe Interact 16: 196-205
15. Fujii J, Ikeda Y (2002) Advances in our understanding of peroxiredoxin, a multifunctional, mammalian redox protein. Redox Rep 7: 123-130
16. Gelhaye E, Rouhier N, Laurent P, Sautiere PE, Martin F, Jacquot JP (2002) Isolation and characterization of an extended thioredoxin h from poplar. Physiol Plant 114: 165-171
17. Gelhaye E, Rouhier N, Vlamis-Gardikas A, Girardet JM, Sautiere PE, Sauzet M, Martin F, Jacquot JP (2003) Identification and characterization of a third thioredoxin h in poplar. Plant Physiol Biochem 41: 629-635
18. Goyer A, Haslekas C, Miginiac-Maslow M, Klein U, Le Marechal P, Jacquot JP, Decottignies P (2002) Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem 269: 272-282
19. Hammad Y, Marechal J, Cournoyer B, Normand P, Domenach AM (2001) Modification of the protein expression pattern induced in the nitrogen-fixing actinomycete Frankia sp. strain ACN14a-tsr by root exudates of its symbiotic host Alnus glutinosa and cloning of the sodF gene. Can J Microbiol 47: 541-547
20. Horling F, Konig J, Dietz KJ (2002) Type IIC peroxiredoxin, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 40: 491-499
21. Horling F, Lamkemeyer P, Konig J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131: 317-325
22. Jacquot JP, Rivera-Madrid R, Marinho P, Kollarova M, Le Marechal P, Miginiac-Maslow M, Meyer Y (1994) Arabidopsis thaliana NAPHP thioredoxin reductase: cDNA characterization and expression of the recombinant protein in Escherichia coli. J Mol Biol 235: 1357-1363
23. Jeong W, Cha MK, Kim IH (2000) Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/alkyl hydroperoxide peroxidase C (AhpC) family. J Biol Chem 275: 2924-2930
24. Kim SJ, Woo JR, Hwang YS, Jeong DG, Shin DH, Kim K, Ryu SE (2003) The tetrameric structure of Haemophilus influenza hybrid Prx5 reveals interactions between electron donor and acceptor proteins. J Biol Chem 278: 10790-10798
25. Kong W, Shiota S, Shi Y, Nakayama H, Nakayama K (2000) A novel peroxiredoxin of the plant Sedum lineare is a homologue of Escherichia coli bacterioferritin comigratory protein (Bcp). Biochem J 351: 107-114
26. Konig J, Baier M, Horling F, Kahmann U, Harris G, Schürmann P, Dietz KJ (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc Natl Acad Sci USA 99: 5738-5743
27. Konig J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz KJ (2003) Reaction mechanism of plant 2-Cys peroxiredoxin: role of the C terminus and the quaternary structure. J Biol Chem 278: 24409-24420
28. Krimm I, Lemaire S, Ruelland E, Miginiac-Maslow M, Jacquot JP, Hirasawa M, Knaff DB, Lancelin JM (1998) The single mutation Trp35→Ala in the 35-40 redox site of Chlamydomonas reinhardtii thioredoxin h affects its biochemical activity and the pH dependence of C36-C39 1H-13C NMR. Eur J Biochem 255: 185-195
29. Laurans F, Pilate G (1999) Histological aspects of a hypersensitive response in poplar to Melamsora larici-populina. Phytopathology 89: 233-238
30. Lee SP, Hwang YS, Kim YJ, Kwon KS, Kim HJ, Kim K, Chae HZ (2001) Cyclophilin a binds to peroxiredoxins and activates its peroxidase activity. J Biol Chem 276: 29826-29832
31. Lemaire SD, Collin V, Keryer E, Quesada A, Miginiac-Maslow M (2003) Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Lett 543: 87-92
32. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593
33. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29: 257-268
34. Menand B, Marechal-Drouard L, Sakamoto W, Dietrich A, Wintz H (1998) A single gene of chloroplast origin codes for mitochondrial and chloroplastic methionyl-tRNA synthetase in Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 11014-11019
35. Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7: 352-356
36. Meyer Y, Vignols F, Reichheld JP (2002) Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol 347: 394-402
37. Miot S, Frey P, Pinon J (1999) Varietal mixture of poplar clones: effects on infection by Melampsora larici-populina and on plant growth. Eur J Forest Pathol 29: 411-123
38. Motohashi K, Kondoh A, Stumpp MT, Hisabori T (2001) Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 98: 11224-11229
39. Niimura Y, Poole LB, Massey V (1995) Amphibacillus xylanus NADH oxidase and Salmonella typhimurium alkyl-hydroperoxide reductase flavoprotein components show extremely high scavenging activity for both alkyl hydroperoxide and hydrogen peroxide in the presence of S. typhimurium alkyl-hydroperoxide reductase 22-kDa protein component. J Biol Chem 270: 25645-25650
40. Park SG, Cha MK, Jeong W, Kim IH (2000) Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J Biol Chem 275: 5723-5732
41. Prinz WA, Aslund F, Holmgren A, Beckwith J (1997) The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J Biol Chem 272: 15661-15667
42. Rouhier N, Gelhaye E, Jacquot JP (2002a) Glutaredoxin-dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism. J Biol Chem 277: 13609-13614
43. Rouhier N, Gelhaye E, Jacquot JP (2002d) Exploring the active site of plant glutaredoxin by site-directed mutagenesis. FEBS Lett 511: 145-149
44. Rouhier N, Gelhaye E, Sautiere PE, Brun A, Laurent P, Tagu D, Gerard J, de Fay E, Meyer Y, Jacquot JP (2001) Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol 127: 1299-1309
45. Rouhier N, Gelhaye E, Sautiere PE, Jacquot JP (2002c) Enhancement of poplar glutaredoxin expression by optimization of the cDNA sequence. Protein Expr Purif 24: 234-241
46. Rouhier N, Jacquot JP (2002b) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74: 259-268
47. Sakamoto A, Tsukamoto S, Yamamoto H, Ueda-Hashimoto M, Takahashi M, Suzuki H, Morikawa H (2003) Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J 33: 841-851
48. Schenk PM, Baumann S, Mattes R, Steinbiss HH (1995) Improved high-level expression system for eukaryotic genes in Escherichia coli using T7 RNA polymerase and rare ArgtRNAs. Biotechniques 19: 196-200
49. Schurmann P (1995) Ferredoxin: thioredoxin system. Methods Enzymol 252: 274-283
50. Schurmann P, Jacquot JP (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371-400
51. Stacy RA, Nordeng TW, Culianez-Macia FA, Aalen RB (1999) The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 19: 1-8
52. Wang PF, Veine DM, Ahn SH, Williams CH (1996) A stable mixed disulfide between thioredoxin reductase and its substrate, thioredoxin: preparation and characterization. Biochemistry 35: 4812-4819
53. Wolff SP (1994) Ferrous ion oxidation of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol 233: 182-189
54. Wong CM, Zhou Y, Kung HF, Jin DY (2002) Cooperation of yeast peroxiredoxins Tsa1p and Tsa2p in the cellular defense against oxidative and nitrosative stress. J Biol Chem 277: 5385-5394
55. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126: 1438-1448